An Overview of Sperm Production

  • Louis Hermo
  • Bernard Robaire


With every heartbeat, men produce approximately 1,000 spermatozoa. Although the regulatory mechanisms are still only partially understood, the remarkably well-organized process needed for this consistent, high level of production of unique haploid cells has been resolved and is presented in the first section of this review. The numerous unique cellular features needed for the extraordinary sperm cell to undertake its function are then discussed.


Spermatogenesis Stem cell renewal Meiosis Spermatid Acrosome Flagellum 


  1. 1.
    Roosen-Runge EC (1962) The process of spermatogenesis in mammals. Biol Rev Camb Philos Soc 37:343-377PubMedCrossRefGoogle Scholar
  2. 2.
    Clermont Y (1972) Kinetics of spermatogenesis in mammals: seminiferous epithelium cycle and spermatogonial renewal. Physiol Rev 52:198-236PubMedGoogle Scholar
  3. 3.
    Kerr JB, Loveland KL, O’Bryan MK, de Kretzer DM (2006) Cytology of the testis and intrinsic control mechanisms. In: Neill JD (ed) Knobil and Neill’s Physiology of Reproduction, vol 1, 3rd edn. Academic Press, Amsterdam, pp 827-947Google Scholar
  4. 4.
    Huckins C, Clermont Y (1968) Evolution of gonocytes in the rat testis during late embryonic and early post-natal life. Arch Anat Histol Embryol 51(1):341-354PubMedGoogle Scholar
  5. 5.
    Griswold MD, McLean D (2006) The Sertoli cell. In: Neill JD (ed) Knobil and Neill’s Physiology of Reproduction, vol 1, 3rd edn. Academic Press, Amsterdam, pp 949-976Google Scholar
  6. 6.
    Skinner MK, Griswold MD (2004) Sertoli cell biology, vol. 1. Academic Press, Amsterdam, 512 pGoogle Scholar
  7. 7.
    Setchell BP, Breed WG (2006) Anatomy, vasculature and innervation of the male reproductive tract. In: Neill JD (ed) Knobil and Neill’s Physiology of Reproduction, vol 1, 3rd edn. Academic Press, Amsterdam, pp 771-825Google Scholar
  8. 8.
    Payne AH, Hardy MP (2007) The Leydig cell in health and disease. Humana Press, Totowa, Amsterdam, 476 pCrossRefGoogle Scholar
  9. 9.
    Steinberger E (1971) Hormonal control of mammalian spermatogenesis. Physiol Rev 51:1-22Google Scholar
  10. 10.
    Skinner MK (1991) Cell-cell interactions in the testis. Endocr Rev 12(1):45-77PubMedCrossRefGoogle Scholar
  11. 11.
    Zirkin BR, Awoniyi C, Griswold MD, Russell LD, Sharpe R (1994) Is FSH required for adult spermatogenesis? J Androl 15:273-276PubMedGoogle Scholar
  12. 12.
    O’Donnell L, Meachem SJ, Stanton PG, McLachlan RI (2006) Endocrine regulation of spermatogenesis. In: Neill JD (ed) Knobil and Neill’s Physiology of Reproduction, vol 1, 3rd edn. Academic Press, Amsterdam, pp 1017-1070Google Scholar
  13. 13.
    Leblond CP, Clermont Y (1952) Definition of the stages of the cycle of the seminiferous epithelium in the rat. Ann N Y Acad Sci 55(4):548-573PubMedCrossRefGoogle Scholar
  14. 14.
    Clermont Y, Trott M (1969) Duration of the cycle of the seminiferous epithelium in the mouse and hamster determined by means of 3H-thymidine and radioautography. Fertil Steril 20:805-817PubMedGoogle Scholar
  15. 15.
    Clermont Y, Leblond CP (1959) Differentiation and renewal of spermatogonia in the monkey, Macacus rhesus. Am J Anat 104:237-273PubMedCrossRefGoogle Scholar
  16. 16.
    Clermont Y (1966) Renewal of spermatogenesis in man. Am J Anat 118:509-524PubMedCrossRefGoogle Scholar
  17. 17.
    Heller CG, Clermont Y (1963) Spermatogenesis in man: an estimate of its duration. Science 140:184-186PubMedCrossRefGoogle Scholar
  18. 18.
    Perey B, Clermont Y, Leblond CP (1961) The wave of the seminiferous epithelium of the rat. Am J Anat 108:47-77CrossRefGoogle Scholar
  19. 19.
    Regaud C (1901) Etudes sur la structure des tubes séminifères et sur la spermatogenèse chez les mammifères. Arch Anat Microsc 4:101-156Google Scholar
  20. 20.
    Brinster RL (2007) Male germline stem cells: from mice to men. Science 316:404-405PubMedCrossRefGoogle Scholar
  21. 21.
    Dym M (1994) Spermatogonial stem cells of the testis. Proc Natl Acad Sci U S A 91:11287-11289PubMedCrossRefGoogle Scholar
  22. 22.
    Brinster RL (2002) Germline stem cell transplantation and transgenesis. Science 296:2174-2176PubMedCrossRefGoogle Scholar
  23. 23.
    de Rooij DG (2001) Proliferation and differentiation of spermatogonial stem cells. Reproduction 121:347-354PubMedCrossRefGoogle Scholar
  24. 24.
    Clermont Y, Bustos-Obregon E (1968) Re-examination of spermatogonial renewal in the rat by means of seminiferous tubules mounted “in toto”. Am J Anat 122:237-247PubMedCrossRefGoogle Scholar
  25. 25.
    Dym M, Clermont Y (1970) Role of spermatogonia in the repair of the seminiferous epithelium following x-irradiation of the rat testis. Am J Anat 128:265-282PubMedCrossRefGoogle Scholar
  26. 26.
    Clermont Y, Hermo L (1975) Spermatogonial stem cells in the albino rat. Am J Anat 142:159-175PubMedCrossRefGoogle Scholar
  27. 27.
    Bartmanska J, Clermont Y (1983) Renewal of type A spermatogonia in adult rats. Cell Tissue Kinet 16:135-143PubMedGoogle Scholar
  28. 28.
    Huckins C (1971) Cell cycle properties of differentiating spermatogonia in adult Sprague-Dawley rats. Cell Tissue Kinet 4:139-154PubMedGoogle Scholar
  29. 29.
    Huckins C (1971) The spermatogonial stem cell population in adult rats. I. Their morphology, proliferation and maturation. Anat Rec 169:533-557PubMedCrossRefGoogle Scholar
  30. 30.
    Huckins C (1971) The spermatogonial stem cell population in adult rats. 3. Evidence for a long-cycling population. Cell Tissue Kinet 4:335-349PubMedGoogle Scholar
  31. 31.
    Huckins C (1971) The spermatogonial stem cell population in adult rats II. A radioautographic analysis of their cell cycle properties. Cell Tissue Kinet 4:313-334PubMedGoogle Scholar
  32. 32.
    de Rooij DG, Grootegoed JA (1998) Spermatogonial stem cells. Curr Opin Cell Biol 10:694-701PubMedCrossRefGoogle Scholar
  33. 33.
    Yoshida S, Takakura A, Ohbo K, Abe K, Wakabayashi J, Yamamoto M, Suda T, Nabeshima Y (2004) Neurogenin3 delineates the earliest stages of spermatogenesis in the mouse testis. Dev Biol 269:447-458PubMedCrossRefGoogle Scholar
  34. 34.
    Roosen-Runge EC, Barlow FD (1953) Quantitative studies on human spermatogenesis. I. Spermatogonia. Am J Anat 93(2):143-169PubMedCrossRefGoogle Scholar
  35. 35.
    Mancini RE, Narbaitz R, Lavieri JC (1960) Origin and development of the germinative epithelium and Sertoli cells in the human testis: cytological, cytochemical, and quantitative study. Anat Rec 136:477-489PubMedCrossRefGoogle Scholar
  36. 36.
    Rowley MJ, Berlin JD, Heller CG (1971) The ultrastructure of four types of human spermatogonia. Z Zellforsch Mikrosk Anat 112(2):139-157PubMedCrossRefGoogle Scholar
  37. 37.
    Schulze W (1978) Light and electron microscope studies of the morphology of A spermatogonia in men with normal spermatogenesis and in patients treated with antiandrogens. Andrologia 10(4):307-320PubMedCrossRefGoogle Scholar
  38. 38.
    Oakberg EF, Gosslee DG, Huckins C, Cummings CC (1986) Do spermatogonial stem cells have a circadian rhythm? Cell Tissue Kinet 19:367-375PubMedGoogle Scholar
  39. 39.
    Ehmcke J, Schlatt S (2006) A revised model for spermatogonial expansion in man: lessons from non-human primates. Reproduction 132(5):673-680PubMedCrossRefGoogle Scholar
  40. 40.
    Clermont Y (1962) Quantitative analysis of spermatogenesis of the rat: a revised model for the renewal of spermatogonia. Am J Anat 111:111-129PubMedCrossRefGoogle Scholar
  41. 41.
    Huckins C (1978) Spermatogonial intercellular bridges in whole-mounted seminiferous tubules from normal and irradiated rodent testes. Am J Anat 153(1):97-121PubMedCrossRefGoogle Scholar
  42. 42.
    Blanco-Rodríguez J, Martínez-García C (1996) Spontaneous germ cell death in the testis of the adult rat takes the form of apoptosis: re-evaluation of cell types that exhibit the ability to die during spermatogenesis. Cell Prolif 29:13-31PubMedCrossRefGoogle Scholar
  43. 43.
    Brinkworth MH, Weinbauer GF, Schlatt S, Nieschlag E (1995) Identification of male germ cells undergoing apoptosis in adult rats. J Reprod Fertil 105:25-33PubMedCrossRefGoogle Scholar
  44. 44.
    Cai L, Hales BF, Robaire B (1997) Induction of apoptosis in the germ cells of adult male rats after exposure to cyclophosphamide. Biol Reprod 56:1490-1497PubMedCrossRefGoogle Scholar
  45. 45.
    Blanco-Rodríguez J, Martínez-García C (1998) Apoptosis pattern elicited by several apoptogenic agents on the seminiferous epithelium of the adult rat testis. J Androl 19:487-497PubMedGoogle Scholar
  46. 46.
    Pentikäinen V, Erkkilä K, Suomalainen L, Otala M, Pentikäinen MO, Parvinen M, Dunkel L (2001) TNFalpha down-regulates the Fas ligand and inhibits germ cell apoptosis in the human testis. J Clin Endocrinol Metab 86:4480-4488PubMedCrossRefGoogle Scholar
  47. 47.
    McKee CM, Ye Y, Richburg JH (2006) Testicular germ cell sensitivity to TRAIL-induced apoptosis is dependent upon p53 expression and is synergistically enhanced by DR5 agonistic antibody treatment. Apoptosis 11:2237-2250PubMedCrossRefGoogle Scholar
  48. 48.
    Richburg JH, Johnson KJ, Schoenfeld HA, Meistrich ML, Dix DJ (2002) Defining the cellular and molecular mechanisms of toxicant action in the testis. Toxicol Lett 135:167-183PubMedCrossRefGoogle Scholar
  49. 49.
    Sugiyama N, Obinata M, Matsui Y (2001) Bcl-2 inhibits apoptosis of spermatogonia and growth of spermatogonial stem cells in a cell-intrinsic manner. Mol Reprod Dev 58:30-38PubMedCrossRefGoogle Scholar
  50. 50.
    Hackstein JH, Hochstenbach R, Pearson PL (2000) Towards an understanding of the genetics of human male infertility: lessons from flies. Trends Genet 16:565-572PubMedCrossRefGoogle Scholar
  51. 51.
    Cobb J, Handel MA (1998) Dynamics of meiotic prophase I during spermatogenesis: from pairing to division. Semin Cell Dev Biol 9:445-450PubMedCrossRefGoogle Scholar
  52. 52.
    Handel MA, Sun F (2005) Regulation of meiotic cell divisions and determination of gamete quality: impact of reproductive toxins. Semin Reprod Med 23:213-221PubMedCrossRefGoogle Scholar
  53. 53.
    Solari AJ (1972) Ultrastructure and composition of the synaptonemal complex in spread and negatively stained spermatocytes of the golden hamster and the albino rat. Chromosoma 39: 237-263PubMedCrossRefGoogle Scholar
  54. 54.
    Heyting C, Dietrich AJ, Moens PB, Dettmers RJ, Offenberg HH, Redeker EJ, Vink AC (1989) Synaptonemal complex proteins. Genome 31:81-87PubMedGoogle Scholar
  55. 55.
    Hoyer-Fender S, Costanzi C, Pehrson JR (2000) Histone macroH2A1.2 is concentrated in the XY-body by the early pachytene stage of spermatogenesis. Exp Cell Res 258:254-260PubMedCrossRefGoogle Scholar
  56. 56.
    Liu JY, Dai XH, Zeng XL, Zhang CS, Hao S, Song YC (2005) The relationship between abnormity of synaptonemal complex and male fertility impairment in human. Yi Chuan 27:819-827PubMedGoogle Scholar
  57. 57.
    Sun F, Greene C, Turek PJ, Ko E, Rademaker A, Martin RH (2005) Immunofluorescent synaptonemal complex analysis in azoospermic men. Cytogenet Genome Res 111:366-370PubMedCrossRefGoogle Scholar
  58. 58.
    Geoffroy-Siraudin C, Aknin-Seiffer I, Metzler-Guillemain C, Ghalamoun-Slaimi R, Bonzi MF, Levy R, Guichaoua MR (2007) Meiotic abnormalities in patients bearing complete AZFc deletion of Y chromosome. Hum Reprod 22(6):1567-1572PubMedCrossRefGoogle Scholar
  59. 59.
    Vallente RU, Cheng EY, Hassold TJ (2006) The synaptonemal complex and meiotic recombination in humans: new approaches to old questions. Chromosoma 115:241-249PubMedCrossRefGoogle Scholar
  60. 60.
    Johnston DS, Wright WW, Dicandeloro P, Wilson E, Kopf GS, Jelinsky SA (2008) Stage-specific gene expression is a fundamental characteristic of rat spermatogenic cells and Sertoli cells. Proc Natl Acad Sci U S A 105:8315-8320PubMedCrossRefGoogle Scholar
  61. 61.
    Liang G, Zhang XD, Wang LJ, Sha YS, Zhang JC, Miao SY, Zong SD, Wang LF, Koide SS (2004) Identification of differentially expressed genes of primary spermatocyte against round spermatid isolated from human testis using the laser capture microdissection technique. Cell Res 14:507-512PubMedCrossRefGoogle Scholar
  62. 62.
    Maclean JA 2nd, Wilkinson MF (2005) Gene regulation in spermatogenesis. Curr Top Dev Biol 71:131-197PubMedCrossRefGoogle Scholar
  63. 63.
    Hogeveen KN, Sassone-Corsi P (2006) Regulation of gene expression in post-meiotic male germ cells: CREM-signalling pathways and male fertility. Hum Fertil (Camb) 9:73-79CrossRefGoogle Scholar
  64. 64.
    Elliott DJ, Grellscheid SN (2006) Alternative RNA splicing regulation in the testis. Reproduction 132:811-819PubMedCrossRefGoogle Scholar
  65. 65.
    Yin H, Lin H (2007) An epigenetic activation role of Piwi and a Piwi-associated piRNA in Drosophila melanogaster. Nature 450:304-308PubMedCrossRefGoogle Scholar
  66. 66.
    Hecht NB (1990) Regulation of ‘haploid expressed genes’ in male germ cells. J Reprod Fertil 88:679-693PubMedCrossRefGoogle Scholar
  67. 67.
    Clermont Y, Oko R, Hermo L (1993) Cell biology of mammalian spermatogenesis. In: Desjardins C (ed) Cell and Molecular biology of the testis. Oxford University Press, New York: pp332-376Google Scholar
  68. 68.
    Hecht NB (1995) The making of a spermatozoon: a molecular perspective. Dev Genet 16:95-103PubMedCrossRefGoogle Scholar
  69. 69.
    Kierszenbaum AL, Rivkin E, Tres LL (2007) Molecular biology of sperm head shaping. Soc Reprod Fertil Suppl 65:33-43PubMedGoogle Scholar
  70. 70.
    Susi FR, Leblond CP, Clermont Y (1971) Changes in the golgi apparatus during spermiogenesis in the rat. Am J Anat 130(3):251-267PubMedCrossRefGoogle Scholar
  71. 71.
    Mollenhauer HH, Morré DJ (1978) Polyribosomes associated with forming acrosome membranes in guinea pig spermatids. Science 200:85-86PubMedCrossRefGoogle Scholar
  72. 72.
    Lalli M, Clermont Y (1981) Structural changes of the head components of the rat spermatid during late spermiogenesis. Am J Anat 160:419-434PubMedCrossRefGoogle Scholar
  73. 73.
    Moreno RD, Alvarado CP (2006) The mammalian acrosome as a secretory lysosome: new and old evidence. Mol Reprod Dev 73:1430-1434PubMedCrossRefGoogle Scholar
  74. 74.
    Salicioni AM, Platt MD, Wertheimer EV, Arcelay E, Allaire A, Sosnik J, Visconti PE (2007) Signalling pathways involved in sperm capacitation. Soc Reprod Fertil Suppl 65:245-259PubMedGoogle Scholar
  75. 75.
    Olson GE, Winfrey V (1991) Structure-function relationships in the sperm acrosome. Ann N Y Acad Sci 637:240-257PubMedCrossRefGoogle Scholar
  76. 76.
    Clermont Y, Rambourg A (1978) Evolution of the endoplasmic reticulum during rat spermiogenesis. Am J Anat 151(2):191-211PubMedCrossRefGoogle Scholar
  77. 77.
    Fawcett DW, Eddy EM, Phillips DM (1970) Observations on the fine structure and relationships of the chromatoid body in mammalian spermatogenesis. Biol Reprod 2:129-153PubMedCrossRefGoogle Scholar
  78. 78.
    Susi FR, Clermont Y (1970) Fine structural modifications of the rat chromatoid body during spermiogenesis. Am J Anat 129:177-191PubMedCrossRefGoogle Scholar
  79. 79.
    Parvinen M (2005) The chromatoid body in spermatogenesis. Int J Androl 28:189-201PubMedCrossRefGoogle Scholar
  80. 80.
    Kotaja N, Sassone-Corsi P (2007) The chromatoid body: a germ-cell-specific RNA-processing centre. Nat Rev Mol Cell Biol 8:85-90PubMedCrossRefGoogle Scholar
  81. 81.
    Söderström KO, Parvinen M (1976) Transport of material between the nucleus, the chromatoid body and the Golgi complex in the early spermatids of the rat. Cell Tissue Res 168:335-342PubMedCrossRefGoogle Scholar
  82. 82.
    Russell L, Frank B (1978) Ultrastructural characterization of nuage in spermatocytes of the rat testis. Anat Rec 190:79-97PubMedCrossRefGoogle Scholar
  83. 83.
    Breucker H, Schäfer E, Holstein AF (1985) Morphogenesis and fate of the residual body in human spermiogenesis. Cell Tissue Res 240:303-309PubMedCrossRefGoogle Scholar
  84. 84.
    Biggiogera M, Fakan S, Leser G, Martin TE, Gordon J (1990) Immunoelectron microscopical visualization of ribonucleoproteins in the chromatoid body of mouse spermatids. Mol Reprod Dev 26:150-158PubMedCrossRefGoogle Scholar
  85. 85.
    Saunders PT, Millar MR, Maguire SM, Sharpe RM (1992) Stage-specific expression of rat transition protein 2 mRNA and possible localization to the chromatoid body of step 7 spermatids by in situ hybridization using a nonradioactive riboprobe. Mol Reprod Dev 33:385-389PubMedCrossRefGoogle Scholar
  86. 86.
    Moussa F, Oko R, Hermo L (1994) The immunolocalization of small nuclear ribonucleoprotein particles in testicular cells during the cycle of the seminiferous epithelium of the adult rat. Cell Tissue Res 278:363-378PubMedCrossRefGoogle Scholar
  87. 87.
    Werner G, Werner K (1995) Immunocytochemical localization of histone H4 in the chromatoid body of rat spermatids. J Submicrosc Cytol Pathol 27:325-330PubMedGoogle Scholar
  88. 88.
    Oko R, Korley R, Murray MT, Hecht NB, Hermo L (1996) Germ cell-specific DNA and RNA binding proteins p48/52 are expressed at specific stages of male germ cell development and are present in the chromatoid body. Mol Reprod Dev 44:1-13PubMedCrossRefGoogle Scholar
  89. 89.
    Burgos MH, Fawcett DW (1955) Studies on the fine structure of the mammalian testis. I. Differentiation of the spermatids in the cat (Felis domestica). J Biophys Biochem Cytol 1:287-300PubMedCrossRefGoogle Scholar
  90. 90.
    Fawcett DW, Ito S, Slautterback D (1959) The occurrence of intercellular bridges in groups of cells exhibiting synchronous differentiation. J Biophys Biochem Cytol 5:453-460PubMedCrossRefGoogle Scholar
  91. 91.
    Dym M, Fawcett DW (1971) Further observations on the numbers of spermatogonia, spermatocytes, and spermatids connected by intercellular bridges in the mammalian testis. Biol Reprod 4:195-215PubMedGoogle Scholar
  92. 92.
    Braun RE, Behringer RR, Peschon JJ, Brinster RL, Palmiter RD (1989) Genetically haploid spermatids are phenotypically diploid. Nature 337:373-376PubMedCrossRefGoogle Scholar
  93. 93.
    Gondos B, Zemjanis R (1970) Fine structure of spermatogonia and intercellular bridges in Macaca nemestrina. J Morphol 131:431-446PubMedCrossRefGoogle Scholar
  94. 94.
    Greenbaum MP, Yan W, Wu MH, Lin YN, Agno JE, Sharma M, Braun RE, Rajkovic A, Matzuk MM (2006) TEX14 is essential for intercellular bridges and fertility in male mice. Proc Natl Acad Sci U S A 103(13):4982-4987PubMedCrossRefGoogle Scholar
  95. 95.
    Fawcett DW, Anderson WA, Phillips DM (1971) Morphogenetic factors influencing the shape of the sperm head. Dev Biol 26:220-251PubMedCrossRefGoogle Scholar
  96. 96.
    Eddy EM (2006) The spermatozoon. In: Neill JD (ed) Knobil and Neill’s Physiology of Reproduction, vol 1, 3rd edn. Academic Press, Amsterdam, pp 3-54Google Scholar
  97. 97.
    Hecht NB (1998) Molecular mechanisms of male germ cell differentiation. Bioessays 20:555-561PubMedCrossRefGoogle Scholar
  98. 98.
    Kistler WS, Henriksén K, Mali P, Parvinen M (1996) Sequential expression of nucleoproteins during rat spermiogenesis. Exp Cell Res 225:374-381PubMedCrossRefGoogle Scholar
  99. 99.
    Steger K, Klonisch T, Gavenis K, Drabent B, Doenecke D, Bergmann M (1998) Expression of mRNA and protein of nucleoproteins during human spermiogenesis. Mol Hum Reprod 4:939-945PubMedCrossRefGoogle Scholar
  100. 100.
    Sassone-Corsi P (2002) Unique chromatin remodeling and transcriptional regulation in spermatogenesis. Science 296:2176-2178PubMedCrossRefGoogle Scholar
  101. 101.
    Brewer L, Corzett M, Balhorn R (2002) Condensation of DNA by spermatid basic nuclear proteins. J Biol Chem 277:38895-38900PubMedCrossRefGoogle Scholar
  102. 102.
    Balhorn R (2007) The protamine family of sperm nuclear proteins. Genome Biol 8:227PubMedCrossRefGoogle Scholar
  103. 103.
    Queralt R, Adroer R, Oliva R, Winkfein RJ, Retief JD, Dixon GH (1995) Evolution of protamine P1 genes in mammals. J Mol Evol 40:601-607PubMedCrossRefGoogle Scholar
  104. 104.
    McKay DJ, Renaux BS, Dixon GH (1986) Human sperm protamines. Amino-acid sequences of two forms of protamine P2. Eur J Biochem 156:5-8PubMedCrossRefGoogle Scholar
  105. 105.
    Ward WS (1993) Deoxyribonucleic acid loop domain tertiary structure in mammalian spermatozoa. Biol Reprod 48:1193-1201PubMedCrossRefGoogle Scholar
  106. 106.
    Sonnack V, Failing K, Bergmann M (2002) Steger K Expression of hyperacetylated histone H4 during normal and impaired human spermatogenesis. Andrologia 34:384-390PubMedCrossRefGoogle Scholar
  107. 107.
    Churikov D, Zalenskaya IA, Zalensky AO (2004) Male germline-specific histones in mouse and man. Cytogenet Genome Res 105:203-214PubMedCrossRefGoogle Scholar
  108. 108.
    Kimmins S, Sassone-Corsi P (2005) Chromatin remodelling and epigenetic features of germ cells. Nature 434:583-589PubMedCrossRefGoogle Scholar
  109. 109.
    Laberge RM, Boissonneault G (2005) Chromatin remodeling in spermatids: a sensitive step for the genetic integrity of the male gamete. Arch Androl 51:125-133PubMedCrossRefGoogle Scholar
  110. 110.
    Marcon L, Boissonneault G (2004) Transient DNA strand breaks during mouse and human spermiogenesis new insights in stage specificity and link to chromatin remodeling. Biol Reprod 70:910-918PubMedCrossRefGoogle Scholar
  111. 111.
    Pradeepa MM, Rao MR (2007) Chromatin remodeling during mammalian spermatogenesis: role of testis specific histone variants and transition proteins. Soc Reprod Fertil Suppl 63:1-10PubMedGoogle Scholar
  112. 112.
    Choudhary SK, Wykes SM, Kramer JA, Mohamed AN, Koppitch F, Nelson JE, Krawetz SA (1995) A haploid expressed gene cluster exists as a single chromatin domain in human sperm. J Biol Chem 270:8755-8762PubMedCrossRefGoogle Scholar
  113. 113.
    Kramer JA, McCarrey JR, Djakiew D, Krawetz SA (1998) Differentiation: the selective potentiation of chromatin domains. Development 125:4749-4755PubMedGoogle Scholar
  114. 114.
    Wykes SM, Krawetz SA (2003) The structural organization of sperm chromatin. J Biol Chem 278:29471-29477PubMedCrossRefGoogle Scholar
  115. 115.
    Cho YS, Iguchi N, Yang J, Handel MA, Hecht NB (2005) Meiotic messenger RNA and noncoding RNA targets of the RNA-binding protein Translin (TSN) in mouse testis. Biol Reprod 73:840-847PubMedCrossRefGoogle Scholar
  116. 116.
    Morales CR, Wu XQ, Hecht NB (1998) The DNA/RNA-binding protein, TB-RBP, moves from the nucleus to the cytoplasm and through intercellular bridges in male germ cells. Dev Biol 201:113-123PubMedCrossRefGoogle Scholar
  117. 117.
    Ostermeier GC, Dix DJ, Miller D, Khatri P, Krawetz SA (2002) Spermatozoal RNA profiles of normal fertile men. Lancet 360:772-777PubMedCrossRefGoogle Scholar
  118. 118.
    Marcon E, Babak T, Chua G, Hughes T, Moens PB (2008) miRNA and piRNA localization in the male mammalian meiotic nucleus. Chromosome Res 16:243-260PubMedCrossRefGoogle Scholar
  119. 119.
    Lalancette C, Miller D, Li Y, Krawetz SA (2008) Paternal contributions: new functional insights for spermatozoal RNA. J Cell Biochem 104:1570-1579PubMedCrossRefGoogle Scholar
  120. 120.
    Gilbert I, Bissonnette N, Boissonneault G, Vallée M, Robert C (2007) A molecular analysis of the population of mRNA in bovine spermatozoa. Reproduction 133:1073-1086PubMedCrossRefGoogle Scholar
  121. 121.
    Shao X, Tarnasky HA, Schalles U, Oko R, van der Hoorn FA (1997) Interactional cloning of the 84-kDa major outer dense fiber protein Odf84. Leucine zippers mediate associations of Odf84 and Odf27. J Biol Chem 272:6105-6113PubMedCrossRefGoogle Scholar
  122. 122.
    O'Bryan MK, Sebire K, Meinhardt A, Edgar K, Keah HH, Hearn MT, De Kretser DM (2001) Tpx-1 is a component of the outer dense fibers and acrosome of rat spermatozoa. Mol Reprod Dev 58:116-125PubMedCrossRefGoogle Scholar
  123. 123.
    Eddy EM, Toshimori K, O'Brien DA (2003) Fibrous sheath of mammalian spermatozoa. Microsc Res Tech 61:103-115PubMedCrossRefGoogle Scholar
  124. 124.
    Rubin CS (1994) A kinase anchor proteins and the intracellular targeting of signals carried by cyclic AMP. Biochim Biophys Acta 1224:467-479PubMedGoogle Scholar
  125. 125.
    Vijayaraghavan S, Liberty GA, Mohan J, Winfrey VP, Olson GE, Carr DW (1999) Isolation and molecular characterization of AKAP110, a novel, sperm-specific protein kinase A-anchoring protein. Mol Endocrinol 13:705-717PubMedCrossRefGoogle Scholar
  126. 126.
    Miki K, Eddy EM (1999) ingle amino acids determine specificity of binding of protein kinase A regulatory subunits by protein kinase A anchoring proteins. J Biol Chem 274:29057-29062PubMedCrossRefGoogle Scholar
  127. 127.
    Turner RM, Eriksson RL, Gerton GL, Moss SB (1999) Relationship between sperm motility and the processing and tyrosine phosphorylation of two human sperm fibrous sheath proteins, pro-hAKAP82 and hAKAP82. Mol Hum Reprod 5:816-824PubMedCrossRefGoogle Scholar
  128. 128.
    Rawe VY, Ramalho-Santos J, Payne C, Chemes HE, Schatten G (2004) WAVE1, an A-kinase anchoring protein, during mammalian spermatogenesis. Hum Reprod 19:2594-2604PubMedCrossRefGoogle Scholar
  129. 129.
    Clermont Y, Oko R, Hermo L (1990) Immunocytochemical localization of proteins utilized in the formation of outer dense fibers and fibrous sheath in rat spermatids: an electron microscope study. Anat Rec 227:447-457PubMedCrossRefGoogle Scholar
  130. 130.
    Henkel R, Stalf T, Mertens N, Miska W, Schill WB (1994) Outer dense fibres of human spermatozoa: partial characterization and possible physiological functions. Int J Androl 17:68-73PubMedCrossRefGoogle Scholar
  131. 131.
    Phillips DM (1972) Comparative analysis of mammalian sperm motility. J Cell Biol 53:561-573PubMedCrossRefGoogle Scholar
  132. 132.
    Baccetti B, Collodel G, Gambera L, Moretti E, Serafini F, Piomboni P (2005) Fluorescence in situ hybridization and molecular studies in infertile men with dysplasia of the fibrous sheath. Fertil Steril 84:123-129PubMedCrossRefGoogle Scholar
  133. 133.
    El-Alfy M, Moshonas D, Morales CR, Oko R (1999) Molecular cloning and developmental expression of the major fibrous sheath protein (FS 75) of rat sperm. J Androl 20:307-318PubMedGoogle Scholar
  134. 134.
    Brito M, Figueroa J, Maldonado EU, Vera JC, Burzio LO (1989) The major component of the rat sperm fibrous sheath is a phosphoprotein. Gamete Res 22:205-217PubMedCrossRefGoogle Scholar
  135. 135.
    Krisfalusi M, Miki K, Magyar PL, O'Brien DA (2006) Multiple glycolytic enzymes are tightly bound to the fibrous sheath of mouse spermatozoa. Biol Reprod 75:270-278PubMedCrossRefGoogle Scholar
  136. 136.
    Miki K, Qu W, Goulding EH, Willis WD, Bunch DO, Strader LF, Perreault SD, Eddy EM, O'Brien DA (2004) Glyceraldehyde 3-phosphate dehydrogenase-S, a sperm-specific glycolytic enzyme, is required for sperm motility and male fertility. Proc Natl Acad Sci U S A 101:16501-16506PubMedCrossRefGoogle Scholar
  137. 137.
    Oko R, Clermont Y (1991) Origin and distribution of perforatorial proteins during spermatogenesis of the rat: an immunocytochemical study. Anat Rec 230:489-501PubMedCrossRefGoogle Scholar
  138. 138.
    Olson GE, Hamilton DW, Fawcett DW (1976) Isolation and characterization of the perforatorium of rat spermatozoa. J Reprod Fertil 47:293-297PubMedCrossRefGoogle Scholar
  139. 139.
    Oko R, Clermont Y (1988) Isolation, structure and protein composition of the perforatorium of rat spermatozoa. Biol Reprod 39:673-687PubMedCrossRefGoogle Scholar
  140. 140.
    Pouresmaeili F, Morales CR, Oko R (1997) Molecular cloning and structural analysis of the gene encoding PERF 15 protein present in the perinuclear theca of the rat spermatozoa. Biol Reprod 57:655-659PubMedCrossRefGoogle Scholar
  141. 141.
    Yu Y, Xu W, Yi YJ, Sutovsky P, Oko R (2006) The extracellular protein coat of the inner acrosomal membrane is involved in zona pellucida binding and penetration during fertilization: characterization of its most prominent polypeptide (IAM38). Dev Biol 290:32-43PubMedCrossRefGoogle Scholar
  142. 142.
    Ostrowski LE, Blackburn K, Radde KM, Moyer MB, Schlatzer DM, Moseley A, Boucher RC (2002) A proteomic analysis of human cilia: identification of novel components. Mol Cell Proteomics 1:451-465PubMedCrossRefGoogle Scholar
  143. 143.
    Shetty J, Klotz KL, Wolkowicz MJ, Flickinger CJ, Herr JC (2007) Radial spoke protein 44 (human meichroacidin) is an axonemal alloantigen of sperm and cilia. Gene 396:93-107PubMedCrossRefGoogle Scholar

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© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  1. 1.Department of Anatomy and Cell BiologyMcGill UniversityMontrealCanada
  2. 2.Department of Pharmacology and Therapeutics and Obstetrics and GynecologyMcGill UniversityMontrealCanada

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